Prefrontal feature representations drive memory recall

Yadav, Nakul; Noble, Chelsea; Niemeyer, James E.; Terceros, Andrea; Victor, Jonathan D.; Liston, Conor; Rajasethupathy, Priyamvada

doi:10.1038/s41586-022-04936-2

Cited by 32 publications

(20 citation statements)

References 64 publications

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“…Moreover, direct projections from the vHPC provide feedforward inhibition of mPFC neurons to drive fear renewal 12 , a relapse phenomenon not dependent on the RE 33 . Collectively, this provides support for the idea that bidirectional HPC➝mPFC and mPFC➝RE➝HPC interactions act to guide context-appropriate recall of episodic memories 9,63,64 , and that these interactions may be facilitated by neural synchrony in different frequency bands 40,65–67 .…”

Section: Discussionsupporting

confidence: 56%

Thalamic nucleus reuniens coordinates prefrontal-hippocampal synchrony to suppress extinguished fear

Totty

Ramanathan

Jin

et al. 2022

Preprint

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Traumatic events result in vivid and enduring fear memories. Suppressing the retrieval of these memories is central to behavioral therapies for pathological fear. The medial prefrontal cortex (mPFC) and hippocampus (HPC) have been implicated in retrieval suppression, but how mPFC-HPC activity is coordinated during extinction retrieval is unclear. Here we show that after extinction training, coherent theta oscillations (6-9 Hz) in the HPC and mPFC are correlated with the suppression of conditioned freezing in male and female rats. Inactivation of the nucleus reuniens (RE), a thalamic hub interconnecting the mPFC and HPC, reduces extinction-related Fos expression in both the mPFC and HPC, dampens mPFC-HPC theta coherence, and impairs extinction retrieval. Conversely, theta-paced optogenetic stimulation of RE augments fear suppression and reduces relapse of extinguished fear. Collectively, these results demonstrate a novel role for RE in coordinating mPFC-HPC interactions to suppress fear memories after extinction.

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Section: Discussionsupporting

confidence: 56%

Thalamic nucleus reuniens coordinates prefrontal-hippocampal synchrony to suppress extinguished fear

Totty

Ramanathan

Jin

et al. 2022

Preprint

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“…This result is consistent with structural anatomy, as the hippocampus maintains strong, reciprocal connections with the EC and amygdala while connections to neocortex are sparser (Amaral, 2011). Still, given evidence in rodents that some mPFC neurons project directly to the hippocampus (Rajasethupathy et al, 2015), phase-lock to hippocampal theta (Siapas et al, 2005;Hyman et al, 2005;Sirota et al, 2008;Ito et al, 2018;Padilla-Coreano et al, 2019), and are critical for memory retrieval (Rajasethupathy et al, 2015;Yadav et al, 2022), we expected that ACC and OFC neurons would show stronger associations with hippocampal theta than we observed. One possibility is that strong phase-locking to hippocampal theta occurs in the EC and amygdala by default, whereas phase-locking among neurons in the mPFC and other cortical areas is task-dependent.…”

Section: Discussionsupporting

confidence: 89%

MTL neurons phase-lock to human hippocampal theta

Schonhaut

Ramayya

Solomon

et al. 2022

Preprint

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Memory formation depends on neural activity across a network of regions, including the hippocampus and broader medial temporal lobe (MTL). Interactions between these regions have been studied indirectly using functional MRI, but the bases for inter-regional communication at a cellular level remain poorly understood. Here we evaluate the hypothesis that oscillatory currents in the hippocampus synchronize the firing of neurons both within and outside the hippocampus. We recorded extracellular spikes from 1,854 single- and multi-units simultaneously with hippocampal local field potentials (LFPs) in 28 neurosurgical patients who completed virtual navigation experiments. A majority of hippocampal neurons phase-locked to oscillations in the slow (2-4Hz) or fast (6-10Hz) theta bands, with a significant subset exhibiting nested slow theta x beta frequency (13-20Hz) phase-locking. Outside of the hippocampus, phase-locking to hippocampal oscillations occurred only at theta frequencies and primarily among neurons in the entorhinal cortex and amygdala. Extrahippocampal neurons phase-locked to hippocampal theta even when theta did not appear locally. These results indicate that spike-time synchronization with hippocampal theta is a defining feature of neuronal activity in the hippocampus and structurally-connected MTL regions. Theta phase-locking could mediate flexible communication with the hippocampus to influence the content and quality of memories.

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“…We then sought to quantify the difference in temporal divergence activity patterns observed in either context. Such differences have been previously described to be similar in magnitude whether mice learn a rewarding and aversive context as to when they learn either in comparison to an otherwise neutral context (Yadav et al, 2022). To calculate the differential response to context entry (Figure 4B), for each reward or aversive trial, we calculated the change in Z-scored signal from 0 to 2 seconds into the cue zone.…”

Section: Bulk Neural Responsesmentioning

confidence: 84%

Anteromedial Thalamus Gates the Selection & Stabilization of Long-Term Memories

Toader

Regalado

et al. 2023

Preprint

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Memories initially formed in hippocampus gradually stabilize to cortex, over weeks-to-months, for long-term storage. The mechanistic details of this brain re-organization process remain poorly understood. In this study, we developed a virtual-reality based behavioral task and observed neural activity patterns associated with memory reorganization and stabilization over weeks-long timescales. Initial photometry recordings in circuits that link hippocampus and cortex revealed a unique and prominent neural correlate of memory in anterior thalamus that emerged in training and persisted for several weeks. Inhibition of the anteromedial thalamus-to-anterior cingulate cortex projections during training resulted in substantial memory consolidation deficits, and gain amplification more strikingly, was sufficient to enhance consolidation of otherwise unconsolidated memories. To provide mechanistic insights, we developed a new behavioral task where mice form two memories, of which only the more salient memory is consolidated, and also a technology for simultaneous and longitudinal cellular resolution imaging of hippocampus, thalamus, and cortex throughout the consolidation window. We found that whereas hippocampus equally encodes multiple memories, the anteromedial thalamus forms preferential tuning to salient memories, and establishes inter-regional correlations with cortex, that are critical for synchronizing and stabilizing cortical representations at remote time. Indeed, inhibition of this thalamo-cortical circuit while imaging in cortex reveals loss of contextual tuning and ensemble synchrony in anterior cingulate, together with behavioral deficits in remote memory retrieval. We thus identify a thalamo-cortical circuit that gates memory consolidation and propose a mechanism suitable for the selection and stabilization of hippocampal memories into longer term cortical storage.

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Prefrontal feature representations drive memory recall

Cited by 32 publications

References 64 publications

Thalamic nucleus reuniens coordinates prefrontal-hippocampal synchrony to suppress extinguished fear

Thalamic nucleus reuniens coordinates prefrontal-hippocampal synchrony to suppress extinguished fear

MTL neurons phase-lock to human hippocampal theta

Anteromedial Thalamus Gates the Selection & Stabilization of Long-Term Memories

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